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Large Lungworms (Nematoda: Dictyocaulidae) Recovered from the European Bison May Represent a New Nematode Subspecies

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Large Lungworms (Nematoda: Dictyocaulidae) Recovered from the European Bison May Represent a New Nematode Subspecies International Journal for Parasitology: Parasites and Wildlife 13 (2020) 213–220 Contents lists available at ScienceDirect International Journal for Parasitology: Parasites and Wildlife journal homepage: www.elsevier.com/locate/ijppaw Large lungworms (Nematoda: Dictyocaulidae) recovered from the European bison may represent a new nematode subspecies Anna M. Pyziel a,*, Zdzisław Laskowski b, Izabella Dolka c, Marta Kołodziej-Sobocinska´ d, Julita Nowakowska e, Daniel Klich f, Wojciech Bielecki g, Marta Zygowska_ a, Madeleine Moazzami h, Krzysztof Anusz a, Johan Hoglund¨ i a Institute of Veterinary Medicine, Warsaw University of Life Sciences (WULS–SGGW), Department of Food Hygiene and Public Health Protection, Nowoursynowska 159, 02-776, Warsaw, Poland b Polish Academy of Sciences, W. Stefanski´ Institute of Parasitology, Twarda 51/55, 00-818, Warsaw, Poland c Institute of Veterinary Medicine, Warsaw University of Life Sciences (WULS–SGGW), Department of Pathology and Veterinary Diagnostics, Division of Animal Pathology, Nowoursynowska 159c, 02-776, Warsaw, Poland d Mammal Research Institute, Polish Academy of Sciences, Stoczek 1, 17-230, Białowieza,_ Poland e Institute of Biology, University of Warsaw, Laboratory of Electron & Confocal Microscopy, Miecznikowa 1, 20-096, Warsaw, Poland f Institute of Animal Sciences, Warsaw University of Life Sciences (WULS-SGGW), Department of Animal Genetics and Conservation, Ciszewskiego 8, 02-787, Warsaw, Poland g Institute of Veterinary Medicine, Warsaw University of Life Sciences (WULS-SGGW), Department of Pathology and Veterinary Diagnostics, Division of Avian Diseases, Exotic Animals and Fish, Ciszewskiego 8, 02-786, Warsaw, Poland h Swedish University of Agricultural Sciences (SLU), Department of Biomedical Sciences and Veterinary Public Health (BVF), Division of Bacteriology and Food Safety, Box 7035, 75007, Uppsala, Sweden i Swedish University of Agricultural Sciences (SLU), Department of Biomedical Sciences and Veterinary Public Health (BVF), Division of Parasitology, Box 7035, 75007, Uppsala, Sweden ARTICLE INFO ABSTRACT Keywords: Although the Dictyocaulus lungworm, the agent of dictyocaulosis, is one of parasitological threats to European Dictyocaulus viviparus bison, its systematic position remains unclear. The aim of the present study was to evaluate the morphological Bison bonasus features of the lungworm and the pathological lesions it induces, and to analyse mitochondrial (mt) genetic Morphological description markers for systematic and molecular epidemiological studies. The morphological findings indicate that Dic­ Verminous pneumonia tyocaulus lungworms of European bison can be distinguished from those of cattle on the basis of differences in Mitochondrial genetic markers buccal capsule wall length, total body length, and spicules length in males, all of which were significantlylonger in those of European bison. Nucleotide diversity calculated from pairwise sequence alignments of partial cyto­ chrome c oxidase subunit 1 (cox1), cytochrome B (cytB) and NADH dehydrogenase subunit 5 (nad5) of specimens from cattle and European bison varied from 1.7% for nad5, 2.1% for cytB, to 3.7% for cox1 gene. Thus, among the lungworms of European bison and cattle, nad5 and cytB were the most conserved proteins, whereas cox1 was the most diverse. The mt cytB marker gene may be a suitable candidate for distinguishing between the two geno­ types, as nad5 demonstrated the greatest within-genus sequence variation. The lung tissue of infected European bison manifests signs of verminous pneumonia characterized by interstitial pneumonia, bronchitis and bron­ chiolitis. Therefore, it appears that European bison and cattle are infected with slightly diverged, morphologically-different, genotypes of D. viviparus, indicating they belong to two separate worm populations. We propose, therefore, that the lungworm of European bison should be classified as D. viviparus subsp. bisontis. 1. Introduction inhabiting Poland is the European bison, Bison bonasus: the largest terrestrial mammal in Europe; however, it is considered vulnerable to Free-roaming populations of wild ruminants enrich the biodiversity extinction by the International Union for Conservation of Nature - Red of heavily-urbanized landscapes of European countries. A unique bovid List of Threatened Species (IUCN, 2020). The European bison also * Corresponding author. E-mail address: [email protected] (A.M. Pyziel). https://doi.org/10.1016/j.ijppaw.2020.10.002 Received 1 September 2020; Received in revised form 7 October 2020; Accepted 7 October 2020 Available online 24 October 2020 2213-2244/© 2020 The Authors. Published by Elsevier Ltd on behalf of Australian Society for Parasitology. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). A.M. Pyziel et al. International Journal for Parasitology: Parasites and Wildlife 13 (2020) 213–220 suffers from a loss of genetic variation, and is hence more vulnerable to stored in acetone (Eisenback, 1985). The dehydrated specimens were pathogens due to inbreeding depression and the depletion of variation in then subjected to critical-point drying with liquid CO2, their proximal the genes responsible for immunity against parasites (Keller and Waller, endings were cut and mounted on a SEM mounting stub with 2002; Radwan et al., 2010). Dictyocaulosis is a condition affecting double-coated tape, sputter-coated with gold, and examined with the various ungulate hosts, characterized by symptoms of bronchitis, with use of a LEO 1430VP scanning electron microscope. infection leading fatal outcomes in heavily-infected individuals (Demi­ aszkiewicz et al., 2009; Pyziel et al., 2018a). In order to understand the 2.3. DNA extraction, amplification and sequencing risk for cross-transmission between free-roaming European bison and cattle, and to the control the spread of dictyocaulosis, it is essential to Depending on individual intensity of infection, 1–5 male worms from have the potential to correctly identify lungworm species. However, each examined European bison were used for molecular analyses. although some initial studies on European bison-derived lungworms Genomic DNA was extracted individually from 48 adult male lung­ have been published, their systematic position remains unclear (Pyziel, worms (preserved in 70% ethanol) using a Nucleospin tissue DNA 2014, 2018; Pyziel et al., 2017). extraction kit (Macherey-Nagel, Düren, Germany) according to the The small subunit (SSU) rDNA sequence of D. viviparus from Euro­ manufacturer’s protocol. Partial regions of mitochondrial (mt) cox1, pean bison has been found to be generally identical to those from cattle; NADH dehydrogenase subunit 5 (nad5), and cytochrome B (cytB) of the however, the two groups were found to diverge at the internal tran­ worms were amplified by PCR using the following sets of primers: 0 0 scribed spacer (ITS2) region of the ribosomal RNA-array (Pyziel, 2014). LCO1490 (5 -GGT CAA CAA ATC ATA AAG ATA TTG G-3 ) + HC02198 0 0 Additionally, the mt cytochrome c oxidase subunit 1 (cox1) nucleotide (5 -TAA ACT ATC GGG TGA CCA AAA AAT CA-3 ) for cox1 (Folmer 0 0 sequence demonstrates high intraspecific diversity between the two et al., 1994); OP424 (5 -ATG ACT AAT CGT ATT GGG GA-3 ) + OP425 0 0 strains of D. viviparus (Pyziel et al., 2017). However, the mt cytochrome (5 -TAA ACT TCA GGG TGA CCA AAA AAT CA-3 ) for nad5 (Hoglund¨ 0 0 c oxidase subunit 3 (cox3) gene was found as an inefficient mt marker et al., 2006); cytB_F (5 -TGA AAA RGT TAA GAT RRT TGG GAC-3 ) + 0 0 for systematic study on Dictyocaulus spp. (Pyziel et al., 2018b). cytB_R (5 -TTA GGA ATA GCA CGC AAA ATA GC-3 ) for cytB (present The present study examines the morphological features of European study). The primers were designed with the use of FastPCR software, bison lungworm, evaluates its impact on the lung tissue of the host, and version 5.4 (Primer Digital, Helsinki, Finland). identifies the most efficient mt genetic markers for systematic and mo­ PCR was performed in a 2720 thermal cycler (Applied Biosystems, lecular epidemiological studies. Foster City, California) in a volume of 50 μl. Each 50 μl PCR reaction contained 20 μl of Molecular Biology Reagent Water (Sigma-Aldrich, 2. Materials and methods USA), 25 μl Quant-Bio’s AccuStart™ II PCR ToughMix® ( × 2 concen­ tration) (Quantabio, Beverly, USA), 1 μl GelTrack Loading Dye ( × 50 2.1. Specimen collection concentration) (Quantabio, Beverly, USA), 1 μl forward primer (20 mM), 1 μl reverse primer (20 mM), and 2 μl of template DNA. The conditions ◦ A total of 30 male and 35 female adult Dictyocaulus lungworms were for PCR were as follows: 94 C for 2 min to denature the DNA, with 35 ◦ ◦ isolated from the respiratory tract of 15 free-roaming European bison. cycles at 94 C for 40 s (cox1 and nad5) or for 45 s (cytB), 57 C for 45 s ◦ ◦ All European bison had been euthanized for various health reasons in (cox1 and nad5) or 56 C for 60 s (cytB), and 72 C for 30 s (cox1, nad5) Białowieza_ Primeval Forest (n = 8) and Borecka Forest (n = 7) (north- or for 45 s (cytB); with a finalextension of 5 min (cox1, nad5) or 10 min ◦ east Poland) during the years 2017–2019. Lethal control is an element of (cytB) at 72 C to ensure complete amplifications.The PCR product was health monitoring conducted annually. Individuals of weak condition purified with the use of the Nucleospin Gel and PCR Clean-up Kit with general or specific signs of disease (e.g. necrotic inflammation of (Macherey-Nagel, Germany), eluted with 30 μl of Molecular Biology the prepuce) were selected. The formal aspects of conducted annual Reagent Water (Sigma-Aldrich, USA) and sequenced in both directions lethal control was described in Klich et al. (2020). The respiratory tracts by Macrogen Europe (Amsterdam, the Netherlands) with the use of were taken exclusively from animals infected by Dictyocaulus sp. The primers used for amplification (5 mM). The sequences were then trachea, bronchi, and bronchioles were cut open and immerses into assembled into contigs using CodonCode Aligner version 8.0 (Codon­ beakers filled with tap water, the sediment was investigated under a Code Corporation, Massachusetts, USA).
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